Farm size and biosecurity measures associated with Strongylus
vulgaris infection in horses
Summary
Background: Selective anthelmintic treatment, advocated due to
evolving anthelmintic resistance, has been associated with an increase
in Strongylus vulgaris prevalence. Reverting to routine interval
anthelmintic treatments is not viable and therefore, identifying other
management factors correlated with S. vulgaris infection is
vital.
Objectives: To investigate possible risk factors associated
with the presence of S. vulgaris infection in residing horses on
Swedish horse establishments.
Study design: Internet-based questionnaire survey.
Methods: A questionnaire, created using the internet-based
survey platform Netigate, was distributed to owners of equine
establishments throughout Sweden via established equine platforms and
social media channels. The survey was available for response from May 21
until September 1 2022. Questions were closed ended with branching logic
paths.
Results: Four factors were significantly associated withS. vulgaris infection, with an increased odds of infection seen
in livery yards (OR 1.67, 95% CI 1.18-2.36, p = 0.004) and premises
with more than ten residing horses (OR 2.42, 95% CI 1.64-3.56, p
< 0.001). A lower odds of infection was seen in establishments
using quarantine routines (OR 0.69, 95% CI 0.50-0.96, p = 0.03) and
anthelmintic treatment of new horses prior to arrival at the premise (OR
0.37, 95% CI 0.18-0.74, p = 0.005).
Main limitation: Due to the presence of S. vulgarisinfection in the present study being based on S. vulgarisdiagnostics performed at the farm level, any association between faecal
diagnostic use and risk of infection could not be investigated.
Conclusions: Although the use of diagnostics for S.
vulgaris can keep infection rates low, large farms or livery yards with
many different horse owners, and those with low use of biosecurity
measures as regards to new horses arriving at the premise, are
associated with a higher risk of infection.
1. Introduction
As grazing animals, horses are inadvertently exposed to intestinal
parasites, with the majority of horses infected to some degree with
cyathostomins.1-4 However, although considered
ubiquitous in horses with pasture access, clinical disease associated
with cyathostomins is fortunately rare.5 In contrast,Strongylus vulgaris , one of the large strongyles, has
considerably greater pathogenicity, and thrombo-embolic disease with
non-strangulating intestinal infarction caused by this parasite often
has a fatal outcome.6-8 As a result of regular
interval treatments with anthelmintic drugs, the prevalence of S.
vulgaris in Sweden, as in most parts of the world, was radically
reduced from 40-60% in 1979 to a mere 5% in the
1990s.9,10 However, due to the emergence of
anthelmintic drug resistance, selective treatment, i.e. only treating
certain horses based on individual faecal egg counts, often those
excreting greater than 200 eggs per gram faeces (EPG), is
recommended.11-13 Such regimes can greatly reduce the
amount of anthelmintic drugs used, without significantly increasing
parasite pasture contamination caused by
cyathostomins.14 As regards to S. vulgaris ,
however, specific diagnostics are required for detection, and both
Denmark and Sweden, two countries that have strong adherence to
anthelmintic treatment based on faecal diagnostics, have seen a recent
increase in its prevalence.15,16 To this end,
infection with S. vulgaris has been shown to be associated with
the use of a selective anthelmintic treatment strategy, as opposed to
regular treatment of all horses.15,17 Furthermore,
Tydén et al. (2019) demonstrated that excluding specific diagnostics forS. vulgaris was associated with an increased risk of
infection.16 However, other specific risk factors
associated with S. vulgaris infection have yet to be determined.
Since regression to regular interval treatment with anthelmintic drugs
is not acceptable, alternative methods of reducing the risk of large
strongyle infection in horses are crucial. Identifying specific risk
factors for infection will assist in developing strategies other than
regular anthelmintic treatment to protect horses from S. vulgarisinfection. Using an internet-based questionnaire survey, the aim of the
present study was therefore to investigate possible risk factors
associated with the presence of S. vulgaris infection in residing
horses on Swedish horse farms.
2. Materials and methods
A questionnaire designed on the internet-based survey platform Netigate
(netigate.net) was distributed as an internet link made available for
response from May 21 until September 1 2022 on specific nation-wide
equine orientated websites (tidningenridsport.se, hastsverige.se,
hippson.se) (Suppl. Table 1). In addition, awareness of and access to
the questionnaire was achieved through social media channels,
distributed by the authors directly, as well as by the proprietors of
the equine websites named above, after contact with the authors. The
target population was owners or managers of Swedish equine premises with
adequate knowledge to be able to respond to the questions regarding all
residing horses at their establishment, as opposed to individual horse
owners. All questions apart from one, regarding the equine premises’
postal code, were closed ended with pre-determined answer choices. Some
questions were connected by branching logic, where certain answers
opened up new questions, in order for the respondent to only face
relevant queries. Prior to distribution, a test version of the
questionnaire was sent to ten people with professional equine
backgrounds, for control of time for completion and evaluation of the
questions’ clarity.
3. Statistical analyses
The questionnaire data were analysed using a generalized linear additive
model in R v4.3.1 using S. vulgaris findings as response
variable.18 Factors were removed stepwise until only
significant remained and odds ratio was calculated using package autoReg
v0.0.3 and visualized with ggplot2 v 3.4.4.19,20
4. Results
4.1. Questionnaire data
4.1.1. Strongylus vulgaris diagnostics
The questionnaire was completed by a total of 1118 respondents, all of
which were owners or persons responsible for the care of an entire
equine premise and able to answer questions regarding their premise as a
whole. Of these, 378 respondents did not use regular diagnostic tests
for S. vulgaris , precluding knowledge of possible presence of
infection on their establishment, and were therefore not included for
further analysis. Another 23 respondents were excluded because, despite
the use of regular diagnostics for S. vulgaris , they declared a
lack of knowledge of the presence of infection on their premise. Out of
the remaining 717 respondents, 335 reported to have had at least one
horse infected with S. vulgaris over the past 24 months, with the
remaining 382 respondents declaring no horse positive for S.
vulgaris during that same time period, i.e. 47% of the farms using
specific diagnostics for the parasite had detected the infection. Of the
farms that reported to have positive horses for S. vulgaris , the
number of positive horses detected over the previous two years varied as
follows: 42% one horse, 29% two horses, 18% three to four horses and
6% more than four horses. In 5% of farms, the number of positive
horses was unknown. The geographical distribution of all included farms
is depicted in Figure 1. The majority of premises were located in the
southern half of Sweden, which corresponds to the most horse-dense areas
of Sweden.21
4.1.2. Anthelmintic routines
Although excluded from the risk assessment analysis, due to the presence
of S. vulgaris infection over the past 24 months being unknown,
there were some differences noted regarding which anthelmintic routines
were employed on premises that used S. vulgaris diagnostics
(n=717) and those that did not (n=378), as depicted in Figure 2.
Notably, there was less veterinary involvement and a greater use of
routine treatments on establishments that did not use regular extended
diagnostic tests for S. vulgaris . Furthermore, it was more common
for these premises to have no established unified treatment regime.
4.1.3. General description of included premises and management routines
A general description of all establishments using extended diagnostics
for S. vulgaris , including premise type, farm-size and
horse-turnover is shown in Table 1. For a description of anthelmintic
routines and pasture management methods used on these premises, see
Table 2.
4.2. Associations between questionnaire data and the presence ofS. vulgaris infection
In total, four factors were significantly associated with the presence
of S. vulgaris infection on the farm. Of these, two were
farm-related, whereas the other two factors were related to management
practices of new horses arriving at the premise. As such, farm size was
significantly associated with the risk of having had at least one horse
positive for S. vulgaris within the previous 24 months (p
< 0.001), with 2.42 times (95% CI: 1.64-3.56) higher odds of
infection on large premises (> 10 horses), compared with
premises with ten or fewer horses (Figure 3). Furthermore, the presence
of S. vulgaris infection was significantly associated with
premise type, with 1.67 times (95% CI: 1.18-2.36) higher odds of
infection in livery stables compared with other types of equestrian
establishments (p = 0.004). Using quarantine of new horses arriving at
the premise was associated with a significantly lower odds of infection
(OR 0.69 (95% CI: 0.50-0.96), p = 0.03). In addition, anthelmintic
treatment of new horses prior to arrival was associated with a decreased
odds (OR 0.37 (95% CI 0.18-0.74)) of S. vulgaris positive horses
being present on the farm (p = 0.005).
5. Discussion
Sweden, as well as Denmark, are unique countries in that the majority of
equine owners perform anthelmintic treatment of their adult horses based
exclusively on faecal sample results.15,16,22 This
extensive use of faecal diagnostics and consequent knowledge of current
and historic presence of parasite infection on equine premises allows
for the use of survey-based studies. As such, using an internet-based
questionnaire, we demonstrated farm-related risk factors associated with
the presence of S. vulgaris infection in horse farms in Sweden.
Specifically, large premises and livery stables were correlated with a
greater risk of infection. Furthermore, management practices concerning
new horses arriving at the premise influenced the presence of infection,
with the use of quarantine of new horses after arrival and treating new
horses with an anthelmintic drug prior to arrival at the farm associated
with a lowered risk.
To date, most studies investigating risk factors associated with
intestinal parasite infection in horses have focused on cyathostomins
and Parascaris spp. Infection rates in these parasites have shown
a strong association with age, with young individuals more prone to
infection and high parasite burdens.23-26 In addition,
pasture access is significantly correlated with cyathostomin
infection.26-28 In this context, one study showed that
both young age and increase in pasture access were associated with an
increase in both strongyle egg excretion and the presence of S.
vulgaris antibodies.17 In agreement, Stoughton et al.
(2023) found that racehorses had significantly lower odds of having a
positive titer to S. vulgaris , speculated to be due to more
limited grazing time compared with non-racehorses.29However, purposefully restricting access to grazing is not an
appropriate measure to lower infection risk, whereby studies exploring
other management or farm related factors associated with the risk ofS. vulgaris infection are needed.
The present results showed an association between the presence ofS. vulgaris infection and large equine establishments and livery
stables. Similarly, S. vulgaris infection in donkeys was shown to
be significantly associated with herd size, with increasing infection
rates in herds with more than 50 animals. 30Large farm size has also been linked to an increased prevalence ofParascaris infection in young horses, thought to be a result of
higher infection pressures and a greater risk of anthelmintic
resistance.31 Although anthelmintic resistance inS. vulgaris as yet has not been reported, a greater infection
pressure associated with a larger number of residing horses is a
probable explanation for the increased risk of S. vulgarisinfection observed in the present study. Furthermore, most livery
stables in Sweden are so-called DIY yards, where each owner cares for
their own horse, with shared pastures and other facilities. Thus,
speculatively, despite veterinary involvement and regular faecal
testing, the increased odds risk of S. vulgaris infection
demonstrated on such yards may be related to a lack of consensus
regarding anthelmintic routines, such as timing of faecal samples and
anthelmintic treatments.
In the present study, treating horses with an anthelmintic drug before
arrival was associated with a lower odds of S. vulgaris infected
horses at the establishment. Treating horses prior to arrival could
involve a risk of horses being re-infected at the existing premises, and
therefore it is somewhat surprising that this strategy, as opposed to
treating at arrival, appeared to be the most favourable strategy.
However, it is appreciated that the questionnaire did not allow for
further specification as to how horses receiving an anthelmintic drug
prior to arrival were managed after treatment; for example, the use of
separate gravel paddocks or similar could reduce the risk of
re-infection. Further, usage of quarantine practices for new arrivals
lowered infection risk. By not introducing new horses to a shared
pasture immediately at arrival, time is given to treat the horses with
an anthelmintic drug without the risk of prior pasture contamination.
Furthermore, previous studies have shown that applying biosecurity
measures when introducing new horses also decreases the risk of
introducing resistant parasites.32-34
Somewhat surprisingly, no pasture management method in the present study
was found to be significantly associated with the presence of S.
vulgaris infection. Thus, the present study suggests that, at low
infection levels and with regular S. vulgaris diagnostics,
pasture management does not appear to have a major influence on the risk
of S. vulgaris infection. However, the results nonetheless point
to further potential for reducing parasite infection pressures. For
example, similarly to what has been shown in previous surveys, only a
minority of premises in the present study declared to use regular faecal
removal in the summer. 22,35-38 This is regrettable,
given that faecal removal twice weekly has been shown to be highly
effective in reducing parasite infection
pressures.39,40 Furthermore, other management
practices to reduce parasite burdens, such as resting pastures,
ploughing or rotational grazing with another species, were only employed
by a minority of the included farms.
Although it is a major concern that one third of all responders declared
not to make use of regular S. vulgaris diagnostics, previous
studies conducted in Sweden showed an even greater lack of specific
diagnostic usage, suggesting that diagnostics for S. vulgaris ,
although not universal, are becoming increasingly more
commonplace.16,22 To this end, countries where
national legislation enforces prescription only restrictions on
anthelmintic drugs, which includes Sweden as well as Denmark and the
United Kingdom, appear to be experiencing pronounced changes in
anthelmintic treatment strategies, with a clear increase in adherence to
current recommendations.22,41-43
Overall, the number of S. vulgaris positive horses over the past
two year period was low, with only one to two positive horses detected
on the majority of farms that had the infection. A recently published
study, presenting data from the Swedish Veterinary Institute’s parasite
monitoring program during the years 2008-2017, showed between 4-11% of
horses to be positive for S. vulgaris .14 A
substantially higher occurrence was found in the study performed by
Tydén et al. (2019), where 28% of all tested horses were positive forS. vulgaris. 16 A major difference between our
study and that of Tydén et al. (2019) was that the present study was
based purely on questionnaire data. Thus, the infection rate on the
farms that did not use regular diagnostics for S. vulgaris (34%)
was unknown and these farms had to be excluded from further analyses.
Considering that Tydén et al. (2019) demonstrated a 2.9 higher odds of
infection in farms not using diagnostic testing for S. vulgaris ,
the actual number of farms with positive horses in the present study is
likely to have been much greater.16 Moreover, in the
present study, premises that did not use S. vulgaris diagnostics
were less likely to base anthelmintic treatments on faecal samples
and/or veterinary advice, with 27% declaring to routinely treat their
horses 1-4 times per year and 20% reporting either no knowledge of
which anthelmintic routines were used or a lack of consensus in a
defined anthelmintic routine. In contrast, all farms using extended
diagnostics, both with and without positive horses, declared high
veterinary involvement and low use of routine treatment. Thus, further
studies combining questionnaire data with faecal samples and serology
for detecting S. vulgaris infection are needed to fully elucidate
risk factors for infection, including diagnostics and treatment
routines.
In conclusion, the present study appears to support the use of
diagnostics for S. vulgaris to keep infection rates low. However,
infection can still occur, despite regular faecal diagnostic tests for
the parasite, primarily on large farms or livery yards with many
different horse owners, and those with low use of biosecurity measures
as regards to new horses arriving at the premise.
Table 1. Response to questions regarding establishment type and size,
including number of new arrivals, type of housing and pasture access,
expressed as a percentage of the total number of responses for premises
with S. vulgaris positive horses (in bold) (n = 335) and those
without positive horses (n = 382).